Multidetector computed tomography urography (MDCTU) for diagnosing urothelial malignancy

Clinical Radiology (2007) 62, 324e332

PICTORIAL REVIEW

Multidetector computed tomography urography (MDCTU) for diagnosing urothelial malignancy E.M. Anderson, R. Murphy, A.T.M. Rennie, N.C. Cowan* Department of Radiology, The Churchill Hospital, Oxford, UK Received 17 June 2006; received in revised form 25 September 2006; accepted 2 October 2006

Multidetector computed tomography (MDCT) is well established for the detection of stones and renal masses, but more recently MDCT urography (MDCTU) is becoming widely used for examination of the entire urinary tract aimed specifically for diagnosing urothelial lesions. Evidence is rapidly accumulating to support the use of MDCTU in this manner. Familiarity with the MDCTU signs of urothelial malignancy is a prerequisite for optimum radiological practice. This article provides a review of the appearances of transitional cell cancer in the upper urinary tract and bladder. ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction Multidetector computed tomography (MDCT) is established as a sensitive and specific imaging examination for the detection and characterization of stones and renal masses.1e3 Evidence is rapidly accumulating to support the use of MDCT urography (MDCTU) for diagnosing transitional cell carcinoma (TCC) of the upper urinary tract (UUT) but intravenous urography (IVU) is still widely practised, with detection rates for UUT tumours ranging from 43e64%.4e6 Rapid acquisition of thin slices in the excretory phase allows a comprehensive evaluation of the entire urothelium and also provides information with respect to extragenitourinary pathology. Multiplanar reformatted images (MPR) and maximum intensity projection (MIP) and three-dimensional volume rendering (3DVR) of the excretory phase demonstrates lesions in a plane anatomically familiar to the referring clinician and is useful for display. Axial images are still the principal image format used to make a diagnosis.

* Guarantor and correspondent: N.C. Cowan, Department of Radiology, The Churchill Hospital, Oxford OX3 7LJ, UK. Tel.: þ44 01865 741841; fax: þ44 01865 225946. E-mail address: [email protected] (N.C. Cowan).

A consensus has not yet been reached regarding the indications and methods for MDCTU,7 but in the future it is anticipated that MDCTU will be performed more widely. Familiarity with the MDCTU signs of urothelial malignancy is necessary for optimum radiological practice. This article provides a review of the appearance of TCC in the kidney, renal calyces and pelvis, ureters and bladder.

MDCTU technique Images in this series images were obtained using a two bolus, two series technique using an eight or 16 multi-detector CT machine (GE Lightspeed or Siemens Somatom). The method is described below (Table 1). Initial supine images of the abdomen and pelvis are acquired without contrast and this is followed by the administration of 100 ml non-ionic intravenous contrast media (Iopamidol 300 mg/l). After a 10 min interval, 50 ml intravenous contrast medium is administered and after a further 120 s delay, a second set of supine images are acquired of the abdomen and pelvis providing simultaneous nephrographic and excretory phase information.8,9 The initial contrast medium injection is to opacify the collecting system and the second contrast injection, the renal parenchyma. Both sets of images

0009-9260/$ - see front matter ª 2006 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2006.10.008

220 120 1.25e0.625

are reconstructed to 2.5 mm, overlapping by 1.25 mm sections for review. Protocols for four-, eight-, 16- and 64-section machines have been successfully used at other institutions.10e13 In order to detect all renal tract lesions, multiple phases of image acquisition are required. An initial unenhanced phase is followed by a nephrographic phase acquired at least 100 s after contrast medium injection. This is combined with one10,11,14 or two12,13 acquisitions in the excretory phase. The initial unenhanced images are used to detect renal calculi, as the subsequent presence

1.25

10

16.75

1.675 500

512

320

2.5e1.25

325

Top of Bottom of 1.25  8 liver symphysis or kidney

120 190e220 5 5 320 512 1.675 500 10 1.25

16.75

120 170e220 1.25 2.5 320 512 1.675 500 16.75 10 1.25

Bottom of 1.25  8 symphysis Bottom of 1.25  8 symphysis Top of kidney Top of liver

MDCTU-preC (contrast). MDCTUþC (first recon for radiographer review) MDCTUþC (second recon for reporting and three-dimensional display)

End Start Protocol

Table 1

Imaging parameters for MDCTU

Detector array

Section collimation (mm)

Radiation beam collimation (mm)

Table speed (mm/rot)

Pitch

Scan field of view (mm)

Matrix Display field of view (mm)

Section width (mm)

Reconstruction interval (mm)

kV

mA

MDCTU for diagnosing urothelial malignancy

Figure 1 Axial (a) and coronal MPR (b) from MDCTU shows a soft-tissue mass in the right kidney, which encases the upper infundibulum and invades the peri-infundibular fat (arrow). The attenuated calyceal infundibulum can just be seen within the centre of the mass on the axial image, but is much more readily appreciated on the coronal MPR view.

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of intravenous and collecting system contrast media may obscure these. The nephrographic phase has been shown to be the most sensitive for the detection of renal masses.8 Finally, the excretory phase images are required to assess the collecting system, ureters and bladder. In most protocols, the acquisitions of nephrographic and excretory phase images are separate. However, by using two boluses of contrast media these images can be acquired simultaneously.15 The timing of the excretory phase is important; a single, optimally opacified acquisition through

Figure 2 Oblique coronal MIP reformatted image (a) shows a pelviureteric junction TCC as a filling defect within the renal pelvis (arrow). There is evidence of obstruction with pelvicalyceal dilatation. The oblique imaging of the PUJ has produced an apparent narrowing of the ureter distal to the tumour. The axial image (b) confirms that the tumour is located within the renal pelvis and that there is no spread into the surrounding fat (T1/2).

E.M. Anderson et al.

the renal tract is desired to prevent repeated scanning. However, the published series show a wide variation in the timing of this last scan, from 3e15 min.6,11e15 The use of a 10e12 min delay represents a compromise between the extremes, and in terms of urinary opacification, performs comparably well.16 There are a number of strategies to improve ureteric filling. Extrapolating from excretory urography, a number of groups have used abdominal compression.6,13 Although there does appear to be a small advantage, particularly in the improved dilatation of the upper tracts, it remains to be seen

Figure 3 Coronal MIP (a) and axial (b) images of a nonpapillary upper ureteric TCC. Diffuse thickening of the ureteric wall is best depicted on the coronal images (arrow). At the pelviureteric junction the thickening is greatest and an axial view at this level (b) shows the ureter lumen narrowed to a thin slit.

MDCTU for diagnosing urothelial malignancy

if this improves detection of urinary tract pathology. Compression complicates the procedure and may be contraindicated for a number of patients. The use of an intravenous saline bolus, may also produce a slight advantage in the dilatation of the distal ureters11 and pelvicalyceal systems.13 This requires the intravenous infusion of a 250 ml bolus of 0.9% saline after the contrast medium administration. Again this complicates the investigation and the small recorded benefit does not compensate for this. Low-dose frusemide has been found to effect complete or near complete opacification of 30 of 32 renal collecting system and ureters.10 The injection is administered at least 1 min before the injection of contrast medium. The increase in both urine volume and flow improves ureteric distention and may produce a more uniform dilution of excreted contrast medium than with saline infusion.17 MDCTU generates a large number of primary images and this necessitates workstation review. Wide windowing of the excretory phase images is essential, as the high attenuation of urinary contrast medium may obscure small lesions. The thin-section images acquired lend themselves to post-processing. MPR images allow viewing along the long axis of the kidney, collecting system and portions of the ureters. Images displaying the long axis of the ureter may be achieved by the use of curved planar reformats. These images may have additional diagnostic benefit by revealing the relationship between masses and the surrounding tissue or by revealing small lesions, lying within the plane of an axial section. The use of reformatted images is an efficient method of displaying information to clinical colleagues. The coronal plane both resembles the appearance of IVU images, and is a more familiar anatomical plane to non-radiologists. Images displayed in the coronal plane can be manipulated to demonstrate the

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relevant clinical information on a single image, which cannot always be achieved in the axial plane. The coronal plane is often more relevant for preoperative planning. Similarly, the use of MIP images allows the compression of imaging data into a single view that enables the clinicians to appreciate the relevant abnormality.

Radiation risk of MDCTU As with other multiphase abdominopelvic CT techniques, MDCTU can expose the patient to considerable radiation and the risks of medical exposure to ionizing radiation should not be underestimated.18 The dose of radiation is related to number of acquisitions. For example, the fourphase technique of Caoili et al.12 reported a dose of between 25 and 35 mSv, whereas three-phase techniques have reported doses between 1519 or 22 mSv.11 All techniques exceed the dose for IVU, which are 5e1012, 1019 and 11 mSv11, respectively. By reducing the number of acquisitions by using a split-bolus technique we can further reduce the dose. In our experience, this technique has a dose of around 12 mSv, and although this is considerably higher than our IVU dose at 2.5 mSv, it is comparable with the dose of other multiphase techniques, such as liver or pancreas CT, as practised in our department. The radiation dose of MDCTU necessitates careful consideration as to its use. As with all radiological tests involving ionizing radiation, the risks of exposure must be balanced against the pretest probability of the presence of significant pathology. In the case of TCC the most significant risk factors are patient age and the presence of macroscopic, as opposed to microscopic haematuria. Thus for patients under the age of 40 years, an alternative imaging strategy would be undertaken, whereas for

Table 2

TMN staging or transitional cell cancer (TCC) of the urinary tract

TNM

Bladder TCC

Collecting system/renal pelvis TCC

TIS TA T1 T2 T3a T3b T4a T4b

Carcinoma in situ N/A Superficial, limited to mucosa and submucosa Superficial, invasion of muscular wall Deep invasion of muscular wall Perivesical fat invasion Extension to perivesical organs; Invasion of the pelvic and/or abdominal wall

Carcinoma in situ Non-invasive papillary carcinoma Invasion of the subepithelial connective tissue Tumor confined to the muscularis layer Invasion of the renal parenchyma and/or peripelvic soft tissues

N

Lymph node > 10 mm

Lymph node > 10 mm

M

Distant metastases

Distant metastases

Extension beyond the renal capsule

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patients over 40 with macroscopic haematuria, MDCTU would be the initial investigation. Other conditions, such as complicated stone disease, ureteric trauma, including iatrogenic injury and pre- and postoperative assessment of the urinary tract, are other indications that may be appropriate after discussion.

E.M. Anderson et al.

lesions.20,23,24 Upper tract TCC is staged using the TMN system,25 as detailed in Table 2. As MDCTU does not distinguish between the muscle layers it cannot differentiate between T1 and T2 disease. However, it does allow local staging of more advanced disease. The reported accuracy of CT in the staging of upper tract TCC is variable, with

TCC of the renal calyces and pelvis TCC is the most common malignant neoplasm of the urothelium. Risk factors include cigarette smoking, increasing age or exposure to industrial carcinogens, such as aniline dyes, rubber cable or plastics. TCC is 30e50 times more common in the bladder than ureters and renal pelvis, and is often multifocal. Bilateral renal pelvis TCC occurs in between 1 and 5% of cases; patients with a bladder TCC may have an upper tract TCC in 3% of cases, whereas 30e40% of upper tract TCCs are associated with a bladder tumour. TCC has two growth patterns: papillary and non-papillary or flat lesions, with the latter divided into invasive and noninvasive. Approximately half of papillary tumours have a base on the epithelium and grow into the lumen, whereas non-papillary tumours usually grow invasively deep into the wall. Calcification of TCC is rare (<3%), and if present, usually shows a diffuse, punctate pattern. TCC may be identified on MDCTU as an enhancing soft-tissue density mass. Although the size and morphology may vary, more uniform enhancement is seen in comparison with renal cell cancers. They are seen as filling defects on the excretory phase. (Figs. 1 and 2) Tumours of the collecting system appear as sessile or pedunculated mass lesions (Fig. 2), though their relationship to the urothelium may only be apparent on MPR views. (Fig. 1b) The obliteration of fat planes within the renal pelvis may indirectly point to a lesion. Although small tumours may be detected (<5 mm), secondary signs of a urothelial lesion such as hydronephrosis or calyceal dilatation may be more apparent. A second type of lesion where circumferential urothelial wall thickening is seen has been described20 (Fig. 3). As this lesion does not directly affect the lumen of the collecting system or ureter, it cannot be detected by either IVU or retrograde ureteropyelography. The precise role of MDCTU for the imaging of the upper tracts remains controversial. It is clear that the IVU is relatively poor at detecting upper tract malignancies, missing up to 40% of tumours,4,21,22 whereas initial results show that MDCTU is both sensitive and specific in the detection of upper tract

Figure 4 Mid-ureteric TCC seen as a homogeneous filling-defect (curved arrowhead) in the axial (a) and coronal plane (b). Ureteric dilatation distal to the tumour (arrow) produces the goblet or Bergman sign.

MDCTU for diagnosing urothelial malignancy

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a range of 36e83%,26e28 for local disease, and this has led to the questioning of its usefulness. These studies predate the multidetector CT era, and it is reasonable to expect that MDCTU will improve this. MDCTU allows the diagnosis of TCC and staging of both local and extra-genitourinary disease in a single investigation.

TCC of the ureter This is the least common site for TCC. The tumour may be seen as either a filling defect (Fig. 4a) or urothelial thickening (Fig. 3). MPR images may reveal distal ureteric dilatation producing a chalice or goblet-like appearance (Bergman’s sign; Fig. 4b). The distal dilatation is thought to be a direct effect of the tumour, possibly causing intermittent intussusception of the tumour into the distal segment. This is not seen with obstruction due to a stone. Again, initial published results for MDCTU are promising and comparable with retrograde ureteropyelography. Problems in detection may arise where the ureter is not filled with contrast medium or is not dilated.20 An unopacified but dilated ureteric segment should raise suspicion of a tumour, particularly if the dilated segment shows enhancement on the post-contrast images (Fig. 5) If the ureters are not fully opacified, after the first excretory phase series, then repeating the examination with the patient prone may help. This may improve opacification by a gravitational effect or by allowing any peristaltic wave to pass beyond the unopacified segment. It appears most effective at improving opacification of the mid- and lower

Figure 6 A distal ureteric TCC is demonstrated as enhancing thickening of the ureter wall (arrow) on this coronal reformatted view. The ureter has not been opacified but still provides sufficient contrast for the tumour to be clearly seen (arrowhead). Contrast medium from the contra lateral side is seen within the bladder (black arrow).

ureters.11 Gross ureteric dilatation may require a much delayed (>20 min) excretory phase scan to achieve complete ureteric opacification. However, even in the absence of ureteric opacification, the fluid in the ureter and the enhancing tumour may have sufficient contrast media for the latter to be demonstrable (Fig. 6).

TCC of the bladder

Figure 5 Ureterovesical junction TCC. On the axial image the ureter is unopacified but expanded by a uniformly enhancing mass (arrow).

MDCTU may provide a useful adjunct to cystoscopy for detection of bladder carcinoma. Recent work has shown a sensitivity of 93% and specificity of 99%, positive predictive value of 98% and negative predictive value of 97%.29 MDCTU may be useful as an initial non-invasive investigation. Flexible cystoscopy may be reserved for equivocal cases, which comprised 28% of this series of 200 patients, or therapeutic cases. Equivocal cases usually result from incomplete urinary opacification within the bladder or an under-filled bladder. Most tumours produce mural filling defects or focal bladder wall thickening (Fig. 9), whereas diffuse, uniform bladder wall thickening usually represents benign

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Figure 7 defects.

E.M. Anderson et al.

Multifocal bladder TCC seen as small filling

disease such as cystitis or changes related to obstructive uropathy.12 The key to successful identification of wall abnormalities is distension of the bladder and opacification of urine with contrast medium (Fig. 7). Delayed or prone examinations may be appropriate, particularly in cases of incomplete mixing of urine and contrast medium as seen in figure 8, in a case of a TCC in a diverticulum. Diverticula are areas that are relatively inaccessible to cystoscopy and so the role of MDCTU as a diagnostic tool is much more important. The staging of bladder cancer may be achieved either using CT or magnetic resonance imaging (MRI). The most commonly used system today is the TMN (Table 2). CT cannot be used to differentiate the muscle layers of the bladder and so only

Figure 9 Coronal MPR images of multifocal TCC. A tumour is seen in the bladder (arrow) and multiple tumours in the left kidney (arrowhead) (a). Liver (black arrow) and lung (black arrowhead) metastases are clearly seen as low attenuation and ring-enhancing masses (b).

Figure 8 Axial view demonstrating TCC as a filling defect (arrow) in a large bladder diverticulum.

becomes useful in distinguishing T3a from T3b or more aggressive disease (Table 2). CT features that suggest perivesical invasion include loss of the clear interface between the bladder wall and

MDCTU for diagnosing urothelial malignancy

Table 3

331

Bosniak classification of renal cysts

Category

CT features

Work-up

Type I Type II

Simple, uncomplicated cysts One or more thin septa. Thin, mural calcification, fluid contents of increased attenuation. Non-enhancement post-intravenous contrast medium Multiple, type II features Thickened septa, nodular areas of calcification, solid non-enhancing areas Malignant appearance, with solid, enhancing nodules or irregular walls

None None

Type IIF Type III Type IV

adjacent fat, and irregularity or stranding in the perivesical fat. The presence of a soft-tissue mass extending in to the obturator internus muscle or strands of tissues extending through the perivesical fat to the pelvic sidewall indicates T4b disease. Absence of fat planes between adjacent organs such as rectum, prostate, seminal vesicles, uterus or vagina suggests T4a disease. MDCTU has a sensitivity and specificity in the diagnosis of perivesical invasion of 89 and 95%, respectively,30 and has the ability to stage extra-genitourinary disease and examine the upper tracts for synchronous tumours at the same time (Fig. 9).

Renal masses TCC may rarely present as a renal mass. Most carcinomas are solid lesions with attenuation values of 20 HU or greater at unenhanced CT. Small (3 cm diameter) tumours usually have a homogeneous appearance, whereas larger lesions tend to be more heterogeneous owing to haemorrhage or necrosis. It may be difficult to distinguish a renal cell cancer that has invaded the collecting system from a TCC infiltrating the renal substance. The tumour may cause focal obstruction of a calyx, leading to an apparent cystic component. Both may invade the renal vein and inferior vena cava, although this is less common for TCC. As there is an overlap in appearance between TCC and renal cell carcinoma, it is essential to characterize any renal mass. Initially, this is usually as a simple cyst, a complex cyst, or a solid lesion. Cystic renal masses are further classified as benign, equivocal or malignant according to their radiological signs and the Bosniak classification is often used (Table 3).3,31,32 Category I lesions are simple cysts. Category II lesions are slightly more complicated and may contain a few thin septa, thin calcifications, or high-attenuation fluid. Category III lesions are still more complex and may contain areas of wall or septal thickening. Category IV lesions have solid enhancing areas. Category I and II lesions are benign, whereas category III and IV

Follow-up Biopsy or partial nephrectomy Nephrectomy

lesions are possibly malignant and warrant urological assessment. In cystic masses that are difficult to differentiate as category II or category III lesions and in cysts with thick calcifications, category IIF may be used, and these lesions warrant close follow-up.33 In addition, small renal cysts may be wrongly classified as solid lesions due to volume averaging or pseudoenhancement.34 Phantom studies have shown that this is more of a problem with small lesions examined with helical or multidetector CT.35 The use of thin section acquisition, combined with thinner reformatting, can reduce36,37 the impact of volume averaging and allows more accurate Hounsfield values to be calculated. CT is more accurate in the detection of parenchymal masses compared with ultrasound or excretory urography with sensitivities of 94% reported, compared with 67 and 79% for excretory urography and ultrasound respectively.38 CT characterization of a renal mass depends on a combination of unenhanced and contrast-enhanced imaging in the nephrographic phase. The renal parenchyma enhances homogeneously, allowing the best opportunity for discrimination between the normal renal medulla and masses. It allows for the detection of spread of TCC into the renal parenchyma or beyond the renal capsule, T3 or T4 disease, respectively (Table 2). The two bolus, two series imaging protocol permits characterization of masses as simple cysts, complex cysts, or solid neoplasms and their relationship with the collecting system.

Conclusion MDCTU offers significant advantages over other imaging methods in the diagnosis of TCC. It is more sensitive and specific than the IVU and retrograde ureteropyelography for detection of urothelial tumours. The strength of MDCTU is that it is noninvasive and allows complete study of the kidneys, collecting system, ureters and bladder, as well as delineating extra-genitourinary disease, in a single examination.

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